Acessibilidade / Reportar erro

Relationship between early age at menarche, older age at menopause and subtypes of breast cancer: a scoping review

Abstract

Objective

To determine the relationship between early age at menarche, late age at menopause with specific subtypes of breast cancer (BC).

Methods

A literature search was conducted in Embase, Lilacs, PubMed, Scopus, and Scielo databases, following the Joanna Briggs Institute scoping review protocol and answering the question “How early age at menarche or late age at menopause are related to different breast cancer subtypes?”.

Results

A number of 4,003 studies were identified, of which 17 were selected. Most of the included articles found a clear relationship between early menarche, late menopause and some subtypes of BC, mainly, PR+, ER+, luminal, and HER-2 tumors. However, some studies have found a contradictory relationship and one study didn’t find any relationship between them.

Conclusion

A relationship between early age at menarche and advanced age at menopause was observed with some subtypes of breast cancer, since other factors must be considered in its understanding.

Breast neoplasms; Menarche; Menopause; Aged; Age factors

Introduction

Breast cancer (BC) is the second most common type of cancer found among women in Western countries, after non-melanoma skin cancer.11. da Silva BB, Sousa-Esteves FC, Martins RS, Salha CP, Paiva-Melo BN, Moura CS, et al. Clinical and epidemiological profile of women with breast cancer managed in a public referral hospital in northeastern Brazil. Eur J Gynaecol Oncol. 2016;37(6):814-6. It is rare before the age of 35, but its incidence grows rapidly and progressively with aging, being most commonly diagnosed between 40 and 60 years. BC presents a lifetime risk of 12.4% and is the most frequent cancer-related cause of death in women worldwide, representing a significant public health issue in all countries.22. Korzets Y, Yariv O, Mutai R, Moore A, Shochat T, Yerushalmi R, et al. The impact of endogenous estrogen exposures on the characteristics and outcomes of estrogen receptor positive, early breast cancer. Discov Oncol. 2021;12(1):26. doi: 10.1007/s12672-021-00420-x
https://doi.org/10.1007/s12672-021-00420...
,33. Silva PA, Riul SS. Câncer de mama: fatores de risco e detecção precoce. Rev Bras Enferm. 2011;64(6):1016-21. doi: 10.1590/S0034-71672011000600005
https://doi.org/10.1590/S0034-7167201100...
)

Breast cancer results from an interplay between biological, environmental, and genetic factors, such as aging, short breastfeeding periods, family history, nulliparity, late age at first birth, postmenopausal hormone replacement therapy, hysterectomy in late menopause, the expression of the XRCC3 gene and high body mass index (BMI).22. Korzets Y, Yariv O, Mutai R, Moore A, Shochat T, Yerushalmi R, et al. The impact of endogenous estrogen exposures on the characteristics and outcomes of estrogen receptor positive, early breast cancer. Discov Oncol. 2021;12(1):26. doi: 10.1007/s12672-021-00420-x
https://doi.org/10.1007/s12672-021-00420...
,44. Su CH, Chang WS, Hu PS, Hsiao CL, Ji HX, Liao CH, et al. Contribution of DNA double-strand break repair gene XRCC3 genotypes to triple-negative breast cancer risk. Cancer Genom Proteom. 2015;12(6):359-67.,55. Li H, Sun X, Miller E, Wang Q, Tao P, Liu L, et al. BMI, reproductive factors, and breast cancer molecular subtypes: a case-control study and meta-analysis. J Epidemiol. 2017;27(4):143-51. doi: 10.1016/j.je.2016.05.002
https://doi.org/10.1016/j.je.2016.05.002...
Early age at menarche and older age at menopause, have also been pointed as risk factors for the development of BC due to extended exposition to steroid hormones, such as estrogens.44. Su CH, Chang WS, Hu PS, Hsiao CL, Ji HX, Liao CH, et al. Contribution of DNA double-strand break repair gene XRCC3 genotypes to triple-negative breast cancer risk. Cancer Genom Proteom. 2015;12(6):359-67.,66. Collaborative Group on Hormonal Factors in Breast Cancer. Menarche, menopause, and breast cancer risk: individual participant meta-analysis, including 118 964 women with breast cancer from 117 epidemiological studies. Lancet Oncol. 2012;13(11):1141-51. doi: 10.1016/S1470-2045(12)70425-4
https://doi.org/10.1016/S1470-2045(12)70...

7. Actis AM, Bergoc RM, Quartucci Á, Outomuro D. Factores de riesgo convencionales y emergentes en cáncer de mama: un estudio en pacientes posmenopáusicas. Rev Chil Obstet Ginecol. 2009;74(3):135-42. doi: 10.4067/S0717-75262009000300002
https://doi.org/10.4067/S0717-7526200900...
-88. Chen L, Li CI, Tang MT, Porter P, Hill DA, Wiggins CL, et al. Reproductive factors and risk of luminal, HER2-overexpressing, and triple-negative breast cancer among multiethnic women. Cancer Epidemiol Biomarkers Prev. 2016;25(9):1297-304. doi: 10.1158/1055-9965.EPI-15-1104
https://doi.org/10.1158/1055-9965.EPI-15...
It should be noted that the ages at menarche and menopause vary among individuals and are also influenced by complex social, environmental, and genetic factors.22. Korzets Y, Yariv O, Mutai R, Moore A, Shochat T, Yerushalmi R, et al. The impact of endogenous estrogen exposures on the characteristics and outcomes of estrogen receptor positive, early breast cancer. Discov Oncol. 2021;12(1):26. doi: 10.1007/s12672-021-00420-x
https://doi.org/10.1007/s12672-021-00420...
,99. Coignet MV, Zirpoli GR, Roberts MR, Khoury T, Bandera EV, Zhu Q, et al. Genetic variations, reproductive aging, and breast cancer risk in African American and European American women: The Women's Circle of Health Study. PLoS One. 2017;12(10):e0187205. doi: 10.1371/journal.pone.0187205
https://doi.org/10.1371/journal.pone.018...
Each 1-year delay in menopause increases the risk of BC by 3%, and each 1-year delay in menarche decreases the risk of BC by 5%.22. Korzets Y, Yariv O, Mutai R, Moore A, Shochat T, Yerushalmi R, et al. The impact of endogenous estrogen exposures on the characteristics and outcomes of estrogen receptor positive, early breast cancer. Discov Oncol. 2021;12(1):26. doi: 10.1007/s12672-021-00420-x
https://doi.org/10.1007/s12672-021-00420...
,1010. Sun YS, Zhao Z, Yang ZN, Xu F, Lu HJ, Zhu ZY, et al. Risk factors and preventions of breast cancer. Int J Biol Sci. 2017;13(11):1387-97. doi: 10.7150/ijbs.21635
https://doi.org/10.7150/ijbs.21635...

Classifying BC is crucial for defining its prognosis and treatment. The World Health Organization (WHO) proposes histological and molecular classifications. Regarding histological aspects, several subtypes of BC can be found, being ductal (in situ and invasive) and lobular (in situ and invasive) carcinomas are the most prevalent. Molecular classification is made by the expression of some surface molecules, such as estrogen receptors (ER), progesterone receptors (PR) and the human epidermal growth factor receptor 2 (HER2), that may be present or not in different subtypes of BC. Also, the degree of expression of the cellular proliferation biomarker Ki-67 is considered. Consequently, BC can be classified as luminal A (ER+ and/or PR+, HER2 - and low expression of Ki-67), luminal B (ER+ and/or PR+, HER2- and high expression of Ki-67), HER2 (ER-, PR- and HER2+) and triple negative (ER-, PR- and HER2-).1111. Wysocka J. New WHO classification of breast tumours - as published in 2019. Nowotwory J Oncol. 2020;70(6):250-2. doi: 10.5603/NJO.a2020.0038
https://doi.org/10.5603/NJO.a2020.0038...

This scoping review aims to map and synthesize the relationship between early age at menarche and late age at menopause with the risk of specific subtypes of BC.

Methods

The present study is a scoping literature review, which allows a broad and comprehensive view of records on a respective topic and enables the synthesis of relevant evidence that addresses and informs clinical practice and identifies existing gaps in knowledge. This study follows the proposal of the Joanna Briggs Institute.1212. Peters MD, Marnie C, Tricco AC, Pollock D, Munn Z, Alexander L, et al. Updated methodological guidance for the conduct of scoping reviews. JBI Evid Implement. 2021;19(1):3-10.

Eligible studies were those performed with premenopausal or postmenopausal women with the diagnosis of BC, that contained data regarding age at menarche and age at menopause. After a detailed search, we found multiple subtypes of classifications, as well as multiple age thresholds for early/late menarche and early/late menopause.

The Population, Concept, and Context (PCC) strategy was used to formulate the guiding research question and the search strategy. Thus, we defined “P” as women with BC; “C” as the relationship between early age at menarche or late age at menopause with different BC subtypes; and the last “C” as data found in articles published in the previous ten years. Considering this definition, the following guiding question was formulated: “How early age at menarche or late age at menopause are related to different breast cancer subtypes?”. The included articles had to contain the three elements of the PCC strategy, answer the research question, and be written in English, Portuguese or Spanish, from January 1st, 2013, until October 20th, 2022. Articles written in other languages, in different time frames, that did not answer the guiding question, case reports, congress abstracts, book chapters, guidelines, roundups, expert opinions, brochures, published in non-indexed sources and reviews were excluded. However, the inclusion criteria were modified as the researchers became more acquainted with the available evidence, as this is possible in scoping reviews.1313. Anderson JK, Howarth E, Vainre M, Humphrey A, Jones PB, Ford TJ. Advancing methodology for scoping reviews: recommendations arising from a scoping literature review (SLR) to inform transformation of Children and Adolescent Mental Health Services. BMC Med Res Methodol. 2020;20(1):242. doi: 10.1186/s12874-020-01127-3
https://doi.org/10.1186/s12874-020-01127...
After a second look at all selected articles for full-text analysis, the exclusion criteria for being review articles was reanalyzed. Some manuscripts initially labeled as reviews were, in reality, reanalyses of cohort, case-only, or case-control data. After careful consideration, we concluded that some articles contained unique sample data and differed from traditional reviews. They presented the results of particular studies exclusively, with geographical and timespan uniqueness. Thus, avoiding the potential bias arising from data duplication if all review articles were included, we designated these studies as “exclusive reanalysis” for inclusion criteria.

The search for articles was conducted between the 15th and 19th of October, 2022 in the following databases: National Library of Medicine (PubMed/MEDLINE), Embase, SCOPUS, Web Of Science, SciElo, and Latin American and Caribbean Health Sciences Literature (LILACS/BVS). For the search, health descriptors (Decs/Mesh), keywords, and their alternative terms, and the Boolean operators OR and AND were used in all databases as presented in chart 1.

Chart 1
Databases and search descriptors selected according to PCC strategy

The selection process was performed by three independent reviewers. Disagreements were resolved through consensus.

As our purpose had a scoping nature, the risk of bias assessing eligible studies was not considered mandatory.1414. Tricco AC, Lillie E, Zarin W, O'Brien KK, Colquhoun H, Levac D, et al. PRISMA Extension for Scoping Reviews (PRISMA-ScR): checklist and explanation. Ann Intern Med. 2018;169(7):467-73. doi: 10.7326/M18-0850
https://doi.org/10.7326/M18-0850...

Results

Based on the initial search, 4,003 articles were identified. Out of this, 2,585 articles were removed for not being published in the last ten years, and 747 were duplicates and were also removed with the support of Mendeley reference manager. Another 440 articles were excluded, for being published in non-indexed journals, 18 were not written in English, Spanish, or Portuguese, 103 were not the selected subtype for analysis, one was a case report, and 318 did not answer the guiding question.

Thus, a total of 231 articles were screened for full-text reading and analysis, 151 were excluded for answering only partially the guiding question, and 72 were excluded for being literature reviews, of which nine were reincluded as “exclusive reanalysis” after a second look for eligibility. 17 articles remained as the final sample, as shown in figure 1.

Figure 1
Flowchart of the study selection process, adapted from PRISMA-ScR

The results are presented in the form of tables and discursive reports. To comply with the methodological rigor, the PRISMA extension tool adapted for scoping reviews was applied.1414. Tricco AC, Lillie E, Zarin W, O'Brien KK, Colquhoun H, Levac D, et al. PRISMA Extension for Scoping Reviews (PRISMA-ScR): checklist and explanation. Ann Intern Med. 2018;169(7):467-73. doi: 10.7326/M18-0850
https://doi.org/10.7326/M18-0850...

Of the 17 included studies, three were conducted in 2013, two in 2014, one in 2015, two in 2016, three in 2017, one in 2018, three in 2020 and two in 2021, as shown in figure 2.22. Korzets Y, Yariv O, Mutai R, Moore A, Shochat T, Yerushalmi R, et al. The impact of endogenous estrogen exposures on the characteristics and outcomes of estrogen receptor positive, early breast cancer. Discov Oncol. 2021;12(1):26. doi: 10.1007/s12672-021-00420-x
https://doi.org/10.1007/s12672-021-00420...
,55. Li H, Sun X, Miller E, Wang Q, Tao P, Liu L, et al. BMI, reproductive factors, and breast cancer molecular subtypes: a case-control study and meta-analysis. J Epidemiol. 2017;27(4):143-51. doi: 10.1016/j.je.2016.05.002
https://doi.org/10.1016/j.je.2016.05.002...
,88. Chen L, Li CI, Tang MT, Porter P, Hill DA, Wiggins CL, et al. Reproductive factors and risk of luminal, HER2-overexpressing, and triple-negative breast cancer among multiethnic women. Cancer Epidemiol Biomarkers Prev. 2016;25(9):1297-304. doi: 10.1158/1055-9965.EPI-15-1104
https://doi.org/10.1158/1055-9965.EPI-15...
,1515. Martinez ME, Wertheim BC, Natarajan L, Schwab R, Bondy M, Daneri-Navarro A, et al. Reproductive factors, heterogeneity, and breast tumor subtypes in women of Mexican descent. Cancer Epidemiol Biomarkers Prev. 2013;22(10):1853-61. doi: 10.1158/1055-9965.EPI-13-0560
https://doi.org/10.1158/1055-9965.EPI-13...

16. Ritte R, Tikk K, Lukanova A, Tjønneland A, Olsen A, Overvad K, et al. Reproductive factors and risk of hormone receptor positive and negative breast cancer: a cohort study. BMC Cancer. 2013;13:584. doi: 10.1186/1471-2407-13-584
https://doi.org/10.1186/1471-2407-13-584...

17. Turkoz FP, Solak M, Petekkaya I, Keskin O, Kertmen N, Sarici F, et al. Association between common risk factors and molecular subtypes in breast cancer patients. Breast. 2013;22(3):344-50. doi: 10.1016/j.breast.2012.08.005
https://doi.org/10.1016/j.breast.2012.08...

18. Cui Y, Deming-Halverson SL, Shrubsole MJ, Beeghly-Fadiel A, Fair AM, Sanderson M, et al. Associations of hormone-related factors with breast cancer risk according to hormone receptor status among white and African American women. Clin Breast Cancer. 2014;14(6):417-25. doi: 10.1016/j.clbc.2014.04.003
https://doi.org/10.1016/j.clbc.2014.04.0...

19. Rosato V, Bosetti C, Negri E, Talamini R, Dal Maso L, Malvezzi M, et al. Reproductive and hormonal factors, family history, and breast cancer according to the hormonal receptor status. Eur J Cancer Prev. 2014;23(5):412-7. doi: 10.1097/CEJ.0b013e3283639f7a
https://doi.org/10.1097/CEJ.0b013e328363...

20. O'Brien KM, Sun J, Sandler DP, DeRoo LA, Weinberg CR. Risk factors for young-onset invasive and in situ breast cancer. Cancer Causes Control. 2015;26(12):1771-8. doi: 10.1007/s10552-015-0670-9
https://doi.org/10.1007/s10552-015-0670-...

21. Sisti JS, Collins LC, Beck AH, Tamimi RM, Rosner BA, Eliassen AH. Reproductive risk factors in relation to molecular subtypes of breast cancer: results from the nurses' health studies. Int J Cancer. 2016;138(10):2346-56. doi: 10.1002/ijc.29968
https://doi.org/10.1002/ijc.29968...

22. Ellingjord-Dale M, Vos L, Tretli S, Hofvind S, Dos-Santos-Silva I, Ursin G. Parity, hormones and breast cancer subtypes - results from a large nested case-control study in a national screening program. Breast Cancer Res. 2017;19(1):10. doi: 10.1186/s13058-016-0798-x
https://doi.org/10.1186/s13058-016-0798-...

23. Mullooly M, Khodr ZG, Dallal CM, Nyante SJ, Sherman ME, Falk R, et al. Epidemiologic risk factors for in situ and invasive breast cancers among postmenopausal women in the National Institutes of Health-AARP Diet and Health Study. Am J Epidemiol. 2017;186(12):1329-40. doi: 10.1093/aje/kwx206
https://doi.org/10.1093/aje/kwx206...

24. Soewoto W, Mudigdo A, Aryandono T, Dirgahayu P. Correlation between duration of estrogen exposure with grading of breast cancer. Bali Med J. 2018;7(3):778-81.

25. John EM, Phipps AI, Hines LM, Koo J, Ingles SA, Baumgartner KB, et al. Menstrual and reproductive characteristics and breast cancer risk by hormone receptor status and ethnicity: The Breast Cancer Etiology in Minorities study. Int J Cancer. 2020;147(7):1808-22. doi: 10.1002/ijc.32923
https://doi.org/10.1002/ijc.32923...

26. Rojas-Lima E, Gamboa-Loira B, Cebrián ME, Rothenberg SJ, López-Carrillo L. A cumulative index of exposure to endogenous estrogens and breast cancer by molecular subtypes in northern Mexican women. Breast Cancer Res Treat. 2020;180(3):791-800. doi: 10.1007/s10549-020-05562-0
https://doi.org/10.1007/s10549-020-05562...

27. Ulgen A, Gurkut O, Li W. Potential predictive factors for breast cancer subtypes from a North Cyprus Cohort Analysis. Cyprus J Med Sci. 2021;5(4):339-49. doi: 10.5152/cjms.2020.2291
https://doi.org/10.5152/cjms.2020.2291...
-2828. Sayed S, Fan S, Moloo Z, Wasike R, Bird P, Saleh M, et al. Breast cancer risk factors in relation to molecular subtypes in breast cancer patients from Kenya. Breast Cancer Res. 2021;23(1):68. doi: 10.1186/s13058-021-01446-3
https://doi.org/10.1186/s13058-021-01446...

Figure 2
Trendline of year distribution of articles

The selected studies were conducted in various sites worldwide. 18 countries contributed to the results. Most studies took place in the United States (n = 7), followed by Italy, Mexico, Norway, Turkey (n = 2), China, Denmark, France, Germany, Greece, Israel, Indonesia, Kenya, Puerto Rico, Spain, Sweden, The Netherlands and United Kingdom (n = 1). Some studies were conducted in only one country (Indonesia, Israel, Kenya, Mexico, USA, Turkey), or multiple countries.

The most commonly used research designs were case-control (n = 7), but there were also cohort (N = 5) and cross-sectional studies (n = 5).

Among the 17 included studies, sample sizes varied from 108 to 30, 680 participants. The populations also differed regarding age and ethnicity, which included different nationalities and ethnicities between countries and within the same country, such as African-Americans and Latin Americans in the USA. The age range could not be specified since the studies did not describe minimum and maximum values.

The characteristics of the selected articles can be seen in chart 2 (which describes the name of the authors, year of publication, country and study design).

Chart 2
Description of the included studies according to authors, year of publication, country, study design, overall population, Breast cancer molecular subtype, Main results and conclusions, definitions of age at menarche and age at menopause

Most of the studies explored molecular subtypes,22. Korzets Y, Yariv O, Mutai R, Moore A, Shochat T, Yerushalmi R, et al. The impact of endogenous estrogen exposures on the characteristics and outcomes of estrogen receptor positive, early breast cancer. Discov Oncol. 2021;12(1):26. doi: 10.1007/s12672-021-00420-x
https://doi.org/10.1007/s12672-021-00420...
,55. Li H, Sun X, Miller E, Wang Q, Tao P, Liu L, et al. BMI, reproductive factors, and breast cancer molecular subtypes: a case-control study and meta-analysis. J Epidemiol. 2017;27(4):143-51. doi: 10.1016/j.je.2016.05.002
https://doi.org/10.1016/j.je.2016.05.002...
,88. Chen L, Li CI, Tang MT, Porter P, Hill DA, Wiggins CL, et al. Reproductive factors and risk of luminal, HER2-overexpressing, and triple-negative breast cancer among multiethnic women. Cancer Epidemiol Biomarkers Prev. 2016;25(9):1297-304. doi: 10.1158/1055-9965.EPI-15-1104
https://doi.org/10.1158/1055-9965.EPI-15...
,1515. Martinez ME, Wertheim BC, Natarajan L, Schwab R, Bondy M, Daneri-Navarro A, et al. Reproductive factors, heterogeneity, and breast tumor subtypes in women of Mexican descent. Cancer Epidemiol Biomarkers Prev. 2013;22(10):1853-61. doi: 10.1158/1055-9965.EPI-13-0560
https://doi.org/10.1158/1055-9965.EPI-13...

16. Ritte R, Tikk K, Lukanova A, Tjønneland A, Olsen A, Overvad K, et al. Reproductive factors and risk of hormone receptor positive and negative breast cancer: a cohort study. BMC Cancer. 2013;13:584. doi: 10.1186/1471-2407-13-584
https://doi.org/10.1186/1471-2407-13-584...

17. Turkoz FP, Solak M, Petekkaya I, Keskin O, Kertmen N, Sarici F, et al. Association between common risk factors and molecular subtypes in breast cancer patients. Breast. 2013;22(3):344-50. doi: 10.1016/j.breast.2012.08.005
https://doi.org/10.1016/j.breast.2012.08...

18. Cui Y, Deming-Halverson SL, Shrubsole MJ, Beeghly-Fadiel A, Fair AM, Sanderson M, et al. Associations of hormone-related factors with breast cancer risk according to hormone receptor status among white and African American women. Clin Breast Cancer. 2014;14(6):417-25. doi: 10.1016/j.clbc.2014.04.003
https://doi.org/10.1016/j.clbc.2014.04.0...
-1919. Rosato V, Bosetti C, Negri E, Talamini R, Dal Maso L, Malvezzi M, et al. Reproductive and hormonal factors, family history, and breast cancer according to the hormonal receptor status. Eur J Cancer Prev. 2014;23(5):412-7. doi: 10.1097/CEJ.0b013e3283639f7a
https://doi.org/10.1097/CEJ.0b013e328363...
,2121. Sisti JS, Collins LC, Beck AH, Tamimi RM, Rosner BA, Eliassen AH. Reproductive risk factors in relation to molecular subtypes of breast cancer: results from the nurses' health studies. Int J Cancer. 2016;138(10):2346-56. doi: 10.1002/ijc.29968
https://doi.org/10.1002/ijc.29968...
,2222. Ellingjord-Dale M, Vos L, Tretli S, Hofvind S, Dos-Santos-Silva I, Ursin G. Parity, hormones and breast cancer subtypes - results from a large nested case-control study in a national screening program. Breast Cancer Res. 2017;19(1):10. doi: 10.1186/s13058-016-0798-x
https://doi.org/10.1186/s13058-016-0798-...
,2424. Soewoto W, Mudigdo A, Aryandono T, Dirgahayu P. Correlation between duration of estrogen exposure with grading of breast cancer. Bali Med J. 2018;7(3):778-81.

25. John EM, Phipps AI, Hines LM, Koo J, Ingles SA, Baumgartner KB, et al. Menstrual and reproductive characteristics and breast cancer risk by hormone receptor status and ethnicity: The Breast Cancer Etiology in Minorities study. Int J Cancer. 2020;147(7):1808-22. doi: 10.1002/ijc.32923
https://doi.org/10.1002/ijc.32923...

26. Rojas-Lima E, Gamboa-Loira B, Cebrián ME, Rothenberg SJ, López-Carrillo L. A cumulative index of exposure to endogenous estrogens and breast cancer by molecular subtypes in northern Mexican women. Breast Cancer Res Treat. 2020;180(3):791-800. doi: 10.1007/s10549-020-05562-0
https://doi.org/10.1007/s10549-020-05562...

27. Ulgen A, Gurkut O, Li W. Potential predictive factors for breast cancer subtypes from a North Cyprus Cohort Analysis. Cyprus J Med Sci. 2021;5(4):339-49. doi: 10.5152/cjms.2020.2291
https://doi.org/10.5152/cjms.2020.2291...
-2828. Sayed S, Fan S, Moloo Z, Wasike R, Bird P, Saleh M, et al. Breast cancer risk factors in relation to molecular subtypes in breast cancer patients from Kenya. Breast Cancer Res. 2021;23(1):68. doi: 10.1186/s13058-021-01446-3
https://doi.org/10.1186/s13058-021-01446...
while a minority of them discussed histological classifications.2020. O'Brien KM, Sun J, Sandler DP, DeRoo LA, Weinberg CR. Risk factors for young-onset invasive and in situ breast cancer. Cancer Causes Control. 2015;26(12):1771-8. doi: 10.1007/s10552-015-0670-9
https://doi.org/10.1007/s10552-015-0670-...
,2323. Mullooly M, Khodr ZG, Dallal CM, Nyante SJ, Sherman ME, Falk R, et al. Epidemiologic risk factors for in situ and invasive breast cancers among postmenopausal women in the National Institutes of Health-AARP Diet and Health Study. Am J Epidemiol. 2017;186(12):1329-40. doi: 10.1093/aje/kwx206
https://doi.org/10.1093/aje/kwx206...
,2424. Soewoto W, Mudigdo A, Aryandono T, Dirgahayu P. Correlation between duration of estrogen exposure with grading of breast cancer. Bali Med J. 2018;7(3):778-81. Notably, there were variations in the definitions of menarche and menopause across the studies, especially concerning the specific age thresholds used to classify early and late occurrence of these events. Additionally, some studies did not provide an explicit definition of menopause,55. Li H, Sun X, Miller E, Wang Q, Tao P, Liu L, et al. BMI, reproductive factors, and breast cancer molecular subtypes: a case-control study and meta-analysis. J Epidemiol. 2017;27(4):143-51. doi: 10.1016/j.je.2016.05.002
https://doi.org/10.1016/j.je.2016.05.002...
,2121. Sisti JS, Collins LC, Beck AH, Tamimi RM, Rosner BA, Eliassen AH. Reproductive risk factors in relation to molecular subtypes of breast cancer: results from the nurses' health studies. Int J Cancer. 2016;138(10):2346-56. doi: 10.1002/ijc.29968
https://doi.org/10.1002/ijc.29968...
,2727. Ulgen A, Gurkut O, Li W. Potential predictive factors for breast cancer subtypes from a North Cyprus Cohort Analysis. Cyprus J Med Sci. 2021;5(4):339-49. doi: 10.5152/cjms.2020.2291
https://doi.org/10.5152/cjms.2020.2291...
while one did not specify what was considered a late menarche.2727. Ulgen A, Gurkut O, Li W. Potential predictive factors for breast cancer subtypes from a North Cyprus Cohort Analysis. Cyprus J Med Sci. 2021;5(4):339-49. doi: 10.5152/cjms.2020.2291
https://doi.org/10.5152/cjms.2020.2291...
Some highlights are pointed out below.

  • Early menarche was commonly defined as that occurring before the age of 13 in most studies;(1515. Martinez ME, Wertheim BC, Natarajan L, Schwab R, Bondy M, Daneri-Navarro A, et al. Reproductive factors, heterogeneity, and breast tumor subtypes in women of Mexican descent. Cancer Epidemiol Biomarkers Prev. 2013;22(10):1853-61. doi: 10.1158/1055-9965.EPI-13-0560
    https://doi.org/10.1158/1055-9965.EPI-13...
    ,1616. Ritte R, Tikk K, Lukanova A, Tjønneland A, Olsen A, Overvad K, et al. Reproductive factors and risk of hormone receptor positive and negative breast cancer: a cohort study. BMC Cancer. 2013;13:584. doi: 10.1186/1471-2407-13-584
    https://doi.org/10.1186/1471-2407-13-584...
    ,1919. Rosato V, Bosetti C, Negri E, Talamini R, Dal Maso L, Malvezzi M, et al. Reproductive and hormonal factors, family history, and breast cancer according to the hormonal receptor status. Eur J Cancer Prev. 2014;23(5):412-7. doi: 10.1097/CEJ.0b013e3283639f7a
    https://doi.org/10.1097/CEJ.0b013e328363...
    ,2222. Ellingjord-Dale M, Vos L, Tretli S, Hofvind S, Dos-Santos-Silva I, Ursin G. Parity, hormones and breast cancer subtypes - results from a large nested case-control study in a national screening program. Breast Cancer Res. 2017;19(1):10. doi: 10.1186/s13058-016-0798-x
    https://doi.org/10.1186/s13058-016-0798-...

    23. Mullooly M, Khodr ZG, Dallal CM, Nyante SJ, Sherman ME, Falk R, et al. Epidemiologic risk factors for in situ and invasive breast cancers among postmenopausal women in the National Institutes of Health-AARP Diet and Health Study. Am J Epidemiol. 2017;186(12):1329-40. doi: 10.1093/aje/kwx206
    https://doi.org/10.1093/aje/kwx206...
    -2424. Soewoto W, Mudigdo A, Aryandono T, Dirgahayu P. Correlation between duration of estrogen exposure with grading of breast cancer. Bali Med J. 2018;7(3):778-81.,2626. Rojas-Lima E, Gamboa-Loira B, Cebrián ME, Rothenberg SJ, López-Carrillo L. A cumulative index of exposure to endogenous estrogens and breast cancer by molecular subtypes in northern Mexican women. Breast Cancer Res Treat. 2020;180(3):791-800. doi: 10.1007/s10549-020-05562-0
    https://doi.org/10.1007/s10549-020-05562...

    27. Ulgen A, Gurkut O, Li W. Potential predictive factors for breast cancer subtypes from a North Cyprus Cohort Analysis. Cyprus J Med Sci. 2021;5(4):339-49. doi: 10.5152/cjms.2020.2291
    https://doi.org/10.5152/cjms.2020.2291...
    -2828. Sayed S, Fan S, Moloo Z, Wasike R, Bird P, Saleh M, et al. Breast cancer risk factors in relation to molecular subtypes in breast cancer patients from Kenya. Breast Cancer Res. 2021;23(1):68. doi: 10.1186/s13058-021-01446-3
    https://doi.org/10.1186/s13058-021-01446...
    )

  • Late menarche definition varied across the studies, with age ranges varying from 12 to 15 years and above;

  • Early menopause was typically defined as that occurring before the age of 48,(22. Korzets Y, Yariv O, Mutai R, Moore A, Shochat T, Yerushalmi R, et al. The impact of endogenous estrogen exposures on the characteristics and outcomes of estrogen receptor positive, early breast cancer. Discov Oncol. 2021;12(1):26. doi: 10.1007/s12672-021-00420-x
    https://doi.org/10.1007/s12672-021-00420...
    ,88. Chen L, Li CI, Tang MT, Porter P, Hill DA, Wiggins CL, et al. Reproductive factors and risk of luminal, HER2-overexpressing, and triple-negative breast cancer among multiethnic women. Cancer Epidemiol Biomarkers Prev. 2016;25(9):1297-304. doi: 10.1158/1055-9965.EPI-15-1104
    https://doi.org/10.1158/1055-9965.EPI-15...
    ,1616. Ritte R, Tikk K, Lukanova A, Tjønneland A, Olsen A, Overvad K, et al. Reproductive factors and risk of hormone receptor positive and negative breast cancer: a cohort study. BMC Cancer. 2013;13:584. doi: 10.1186/1471-2407-13-584
    https://doi.org/10.1186/1471-2407-13-584...
    ,1818. Cui Y, Deming-Halverson SL, Shrubsole MJ, Beeghly-Fadiel A, Fair AM, Sanderson M, et al. Associations of hormone-related factors with breast cancer risk according to hormone receptor status among white and African American women. Clin Breast Cancer. 2014;14(6):417-25. doi: 10.1016/j.clbc.2014.04.003
    https://doi.org/10.1016/j.clbc.2014.04.0...
    ,2020. O'Brien KM, Sun J, Sandler DP, DeRoo LA, Weinberg CR. Risk factors for young-onset invasive and in situ breast cancer. Cancer Causes Control. 2015;26(12):1771-8. doi: 10.1007/s10552-015-0670-9
    https://doi.org/10.1007/s10552-015-0670-...
    ,2222. Ellingjord-Dale M, Vos L, Tretli S, Hofvind S, Dos-Santos-Silva I, Ursin G. Parity, hormones and breast cancer subtypes - results from a large nested case-control study in a national screening program. Breast Cancer Res. 2017;19(1):10. doi: 10.1186/s13058-016-0798-x
    https://doi.org/10.1186/s13058-016-0798-...

    23. Mullooly M, Khodr ZG, Dallal CM, Nyante SJ, Sherman ME, Falk R, et al. Epidemiologic risk factors for in situ and invasive breast cancers among postmenopausal women in the National Institutes of Health-AARP Diet and Health Study. Am J Epidemiol. 2017;186(12):1329-40. doi: 10.1093/aje/kwx206
    https://doi.org/10.1093/aje/kwx206...

    24. Soewoto W, Mudigdo A, Aryandono T, Dirgahayu P. Correlation between duration of estrogen exposure with grading of breast cancer. Bali Med J. 2018;7(3):778-81.

    25. John EM, Phipps AI, Hines LM, Koo J, Ingles SA, Baumgartner KB, et al. Menstrual and reproductive characteristics and breast cancer risk by hormone receptor status and ethnicity: The Breast Cancer Etiology in Minorities study. Int J Cancer. 2020;147(7):1808-22. doi: 10.1002/ijc.32923
    https://doi.org/10.1002/ijc.32923...
    -2626. Rojas-Lima E, Gamboa-Loira B, Cebrián ME, Rothenberg SJ, López-Carrillo L. A cumulative index of exposure to endogenous estrogens and breast cancer by molecular subtypes in northern Mexican women. Breast Cancer Res Treat. 2020;180(3):791-800. doi: 10.1007/s10549-020-05562-0
    https://doi.org/10.1007/s10549-020-05562...
    ) although some studies adopted ages ranging from 50 to 55;(1515. Martinez ME, Wertheim BC, Natarajan L, Schwab R, Bondy M, Daneri-Navarro A, et al. Reproductive factors, heterogeneity, and breast tumor subtypes in women of Mexican descent. Cancer Epidemiol Biomarkers Prev. 2013;22(10):1853-61. doi: 10.1158/1055-9965.EPI-13-0560
    https://doi.org/10.1158/1055-9965.EPI-13...
    ,1717. Turkoz FP, Solak M, Petekkaya I, Keskin O, Kertmen N, Sarici F, et al. Association between common risk factors and molecular subtypes in breast cancer patients. Breast. 2013;22(3):344-50. doi: 10.1016/j.breast.2012.08.005
    https://doi.org/10.1016/j.breast.2012.08...
    ,1919. Rosato V, Bosetti C, Negri E, Talamini R, Dal Maso L, Malvezzi M, et al. Reproductive and hormonal factors, family history, and breast cancer according to the hormonal receptor status. Eur J Cancer Prev. 2014;23(5):412-7. doi: 10.1097/CEJ.0b013e3283639f7a
    https://doi.org/10.1097/CEJ.0b013e328363...
    ,2828. Sayed S, Fan S, Moloo Z, Wasike R, Bird P, Saleh M, et al. Breast cancer risk factors in relation to molecular subtypes in breast cancer patients from Kenya. Breast Cancer Res. 2021;23(1):68. doi: 10.1186/s13058-021-01446-3
    https://doi.org/10.1186/s13058-021-01446...
    )

  • Late menopause was generally defined as that occurring at or after the age of 50, though some studies set the threshold at 45, 55, or even 60 years.

  • These discrepancies highlight the diversity in methodologies used regarding age at menarche and menopause.

Breast cancer classification

In general, the studies included in this review covering histological subtypes of BC followed strictly the 2019 WHO classification of BC and the studies concerning molecular subtypes often follow this same classification as seen in Chart 3. However, in many cases, some articles define tumors by the absence or presence of surface proteins such as ER+, PR-, HER2+.

Chart 3
Molecular classification of breast cancer

Relationships observed

Between the included articles, some studies have found a relationship between BC subtypes only with early age at menarche, or only with late age at menopause, but the majority of them have found a relationship between BC subtypes with both, early age at menarche and with late age at menopause.22. Korzets Y, Yariv O, Mutai R, Moore A, Shochat T, Yerushalmi R, et al. The impact of endogenous estrogen exposures on the characteristics and outcomes of estrogen receptor positive, early breast cancer. Discov Oncol. 2021;12(1):26. doi: 10.1007/s12672-021-00420-x
https://doi.org/10.1007/s12672-021-00420...
,55. Li H, Sun X, Miller E, Wang Q, Tao P, Liu L, et al. BMI, reproductive factors, and breast cancer molecular subtypes: a case-control study and meta-analysis. J Epidemiol. 2017;27(4):143-51. doi: 10.1016/j.je.2016.05.002
https://doi.org/10.1016/j.je.2016.05.002...
,88. Chen L, Li CI, Tang MT, Porter P, Hill DA, Wiggins CL, et al. Reproductive factors and risk of luminal, HER2-overexpressing, and triple-negative breast cancer among multiethnic women. Cancer Epidemiol Biomarkers Prev. 2016;25(9):1297-304. doi: 10.1158/1055-9965.EPI-15-1104
https://doi.org/10.1158/1055-9965.EPI-15...
,1515. Martinez ME, Wertheim BC, Natarajan L, Schwab R, Bondy M, Daneri-Navarro A, et al. Reproductive factors, heterogeneity, and breast tumor subtypes in women of Mexican descent. Cancer Epidemiol Biomarkers Prev. 2013;22(10):1853-61. doi: 10.1158/1055-9965.EPI-13-0560
https://doi.org/10.1158/1055-9965.EPI-13...
,1616. Ritte R, Tikk K, Lukanova A, Tjønneland A, Olsen A, Overvad K, et al. Reproductive factors and risk of hormone receptor positive and negative breast cancer: a cohort study. BMC Cancer. 2013;13:584. doi: 10.1186/1471-2407-13-584
https://doi.org/10.1186/1471-2407-13-584...
,1818. Cui Y, Deming-Halverson SL, Shrubsole MJ, Beeghly-Fadiel A, Fair AM, Sanderson M, et al. Associations of hormone-related factors with breast cancer risk according to hormone receptor status among white and African American women. Clin Breast Cancer. 2014;14(6):417-25. doi: 10.1016/j.clbc.2014.04.003
https://doi.org/10.1016/j.clbc.2014.04.0...

19. Rosato V, Bosetti C, Negri E, Talamini R, Dal Maso L, Malvezzi M, et al. Reproductive and hormonal factors, family history, and breast cancer according to the hormonal receptor status. Eur J Cancer Prev. 2014;23(5):412-7. doi: 10.1097/CEJ.0b013e3283639f7a
https://doi.org/10.1097/CEJ.0b013e328363...

20. O'Brien KM, Sun J, Sandler DP, DeRoo LA, Weinberg CR. Risk factors for young-onset invasive and in situ breast cancer. Cancer Causes Control. 2015;26(12):1771-8. doi: 10.1007/s10552-015-0670-9
https://doi.org/10.1007/s10552-015-0670-...

21. Sisti JS, Collins LC, Beck AH, Tamimi RM, Rosner BA, Eliassen AH. Reproductive risk factors in relation to molecular subtypes of breast cancer: results from the nurses' health studies. Int J Cancer. 2016;138(10):2346-56. doi: 10.1002/ijc.29968
https://doi.org/10.1002/ijc.29968...

22. Ellingjord-Dale M, Vos L, Tretli S, Hofvind S, Dos-Santos-Silva I, Ursin G. Parity, hormones and breast cancer subtypes - results from a large nested case-control study in a national screening program. Breast Cancer Res. 2017;19(1):10. doi: 10.1186/s13058-016-0798-x
https://doi.org/10.1186/s13058-016-0798-...

23. Mullooly M, Khodr ZG, Dallal CM, Nyante SJ, Sherman ME, Falk R, et al. Epidemiologic risk factors for in situ and invasive breast cancers among postmenopausal women in the National Institutes of Health-AARP Diet and Health Study. Am J Epidemiol. 2017;186(12):1329-40. doi: 10.1093/aje/kwx206
https://doi.org/10.1093/aje/kwx206...

24. Soewoto W, Mudigdo A, Aryandono T, Dirgahayu P. Correlation between duration of estrogen exposure with grading of breast cancer. Bali Med J. 2018;7(3):778-81.

25. John EM, Phipps AI, Hines LM, Koo J, Ingles SA, Baumgartner KB, et al. Menstrual and reproductive characteristics and breast cancer risk by hormone receptor status and ethnicity: The Breast Cancer Etiology in Minorities study. Int J Cancer. 2020;147(7):1808-22. doi: 10.1002/ijc.32923
https://doi.org/10.1002/ijc.32923...

26. Rojas-Lima E, Gamboa-Loira B, Cebrián ME, Rothenberg SJ, López-Carrillo L. A cumulative index of exposure to endogenous estrogens and breast cancer by molecular subtypes in northern Mexican women. Breast Cancer Res Treat. 2020;180(3):791-800. doi: 10.1007/s10549-020-05562-0
https://doi.org/10.1007/s10549-020-05562...

27. Ulgen A, Gurkut O, Li W. Potential predictive factors for breast cancer subtypes from a North Cyprus Cohort Analysis. Cyprus J Med Sci. 2021;5(4):339-49. doi: 10.5152/cjms.2020.2291
https://doi.org/10.5152/cjms.2020.2291...

28. Sayed S, Fan S, Moloo Z, Wasike R, Bird P, Saleh M, et al. Breast cancer risk factors in relation to molecular subtypes in breast cancer patients from Kenya. Breast Cancer Res. 2021;23(1):68. doi: 10.1186/s13058-021-01446-3
https://doi.org/10.1186/s13058-021-01446...

29. Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, et al. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA. 2006;295(21):2492-502. doi: 10.1001/jama.295.21.2492
https://doi.org/10.1001/jama.295.21.2492...

30. Cotterchio M, Kreiger N, Theis B, Sloan M, Bahl S. Hormonal factors and the risk of breast cancer according to estrogen- and progesterone-receptor subgroup. Cancer Epidemiol Biomarkers Prev. 2003;12(10):1053-60.

31. Althuis MD, Fergenbaum JH, Garcia-Closas M, Brinton LA, Madigan MP, Sherman ME. Etiology of hormone receptor-defined breast cancer: a systematic review of the literature. Cancer Epidemiol Biomarkers Prev. 2004;13(10):1558-68.

32. Yang XR, Sherman ME, Rimm DL, Lissowska J, Brinton LA, Peplonska B, et al. Differences in risk factors for breast cancer molecular subtypes in a population-based study. Cancer Epidemiol Biomarkers Prev. 2007;16(3):439-43. doi: 10.1158/1055-9965.EPI-06-0806
https://doi.org/10.1158/1055-9965.EPI-06...

33. Phipps AI, Chlebowski RT, Prentice R, McTiernan A, Wactawski-Wende J, Kuller LH, et al. Reproductive history and oral contraceptive use in relation to risk of triple-negative breast cancer. J Natl Cancer Inst. 2011;103(6):470-7. doi: 10.1093/jnci/djr030
https://doi.org/10.1093/jnci/djr030...
-3434. Tamimi RM, Colditz GA, Hazra A, Baer HJ, Hankinson SE, Rosner B, et al. Traditional breast cancer risk factors in relation to molecular subtypes of breast cancer. Breast Cancer Res Treat. 2011;131(1):159-67. doi: 10.1007/s10549-011-1702-0
https://doi.org/10.1007/s10549-011-1702-...
Finally, only one did not find a relationship between BC subtypes with the age at menarche or age at menopause.1717. Turkoz FP, Solak M, Petekkaya I, Keskin O, Kertmen N, Sarici F, et al. Association between common risk factors and molecular subtypes in breast cancer patients. Breast. 2013;22(3):344-50. doi: 10.1016/j.breast.2012.08.005
https://doi.org/10.1016/j.breast.2012.08...

An earlier age at menarche has been related to a higher risk of PR+/ER+ tumors, luminal tumors, and lobular tumors. In Parallel, one study showed that an early age at menarche was a risk factor for presenting BC earlier and with a worse prognosis, while another one, showed that a late age at menarche would be protective against BC, but none of them mentioned a specific subtype of BC. Furthermore, some studies have shown that late age at menarche was related to a reduced risk for ER+ BC only, ER+PR+, Luminal A, Luminal B, HR+/HER2- and for triple negative. Finally, this same late age at menarche was related to a higher risk of ER-PR- and ER+PR+ tumors, ER- tumors and HR+/HR- tumors according to other studies.22. Korzets Y, Yariv O, Mutai R, Moore A, Shochat T, Yerushalmi R, et al. The impact of endogenous estrogen exposures on the characteristics and outcomes of estrogen receptor positive, early breast cancer. Discov Oncol. 2021;12(1):26. doi: 10.1007/s12672-021-00420-x
https://doi.org/10.1007/s12672-021-00420...
,55. Li H, Sun X, Miller E, Wang Q, Tao P, Liu L, et al. BMI, reproductive factors, and breast cancer molecular subtypes: a case-control study and meta-analysis. J Epidemiol. 2017;27(4):143-51. doi: 10.1016/j.je.2016.05.002
https://doi.org/10.1016/j.je.2016.05.002...
,1616. Ritte R, Tikk K, Lukanova A, Tjønneland A, Olsen A, Overvad K, et al. Reproductive factors and risk of hormone receptor positive and negative breast cancer: a cohort study. BMC Cancer. 2013;13:584. doi: 10.1186/1471-2407-13-584
https://doi.org/10.1186/1471-2407-13-584...
,1818. Cui Y, Deming-Halverson SL, Shrubsole MJ, Beeghly-Fadiel A, Fair AM, Sanderson M, et al. Associations of hormone-related factors with breast cancer risk according to hormone receptor status among white and African American women. Clin Breast Cancer. 2014;14(6):417-25. doi: 10.1016/j.clbc.2014.04.003
https://doi.org/10.1016/j.clbc.2014.04.0...

19. Rosato V, Bosetti C, Negri E, Talamini R, Dal Maso L, Malvezzi M, et al. Reproductive and hormonal factors, family history, and breast cancer according to the hormonal receptor status. Eur J Cancer Prev. 2014;23(5):412-7. doi: 10.1097/CEJ.0b013e3283639f7a
https://doi.org/10.1097/CEJ.0b013e328363...
-2020. O'Brien KM, Sun J, Sandler DP, DeRoo LA, Weinberg CR. Risk factors for young-onset invasive and in situ breast cancer. Cancer Causes Control. 2015;26(12):1771-8. doi: 10.1007/s10552-015-0670-9
https://doi.org/10.1007/s10552-015-0670-...
,2222. Ellingjord-Dale M, Vos L, Tretli S, Hofvind S, Dos-Santos-Silva I, Ursin G. Parity, hormones and breast cancer subtypes - results from a large nested case-control study in a national screening program. Breast Cancer Res. 2017;19(1):10. doi: 10.1186/s13058-016-0798-x
https://doi.org/10.1186/s13058-016-0798-...
,2424. Soewoto W, Mudigdo A, Aryandono T, Dirgahayu P. Correlation between duration of estrogen exposure with grading of breast cancer. Bali Med J. 2018;7(3):778-81.,2626. Rojas-Lima E, Gamboa-Loira B, Cebrián ME, Rothenberg SJ, López-Carrillo L. A cumulative index of exposure to endogenous estrogens and breast cancer by molecular subtypes in northern Mexican women. Breast Cancer Res Treat. 2020;180(3):791-800. doi: 10.1007/s10549-020-05562-0
https://doi.org/10.1007/s10549-020-05562...

27. Ulgen A, Gurkut O, Li W. Potential predictive factors for breast cancer subtypes from a North Cyprus Cohort Analysis. Cyprus J Med Sci. 2021;5(4):339-49. doi: 10.5152/cjms.2020.2291
https://doi.org/10.5152/cjms.2020.2291...
-2828. Sayed S, Fan S, Moloo Z, Wasike R, Bird P, Saleh M, et al. Breast cancer risk factors in relation to molecular subtypes in breast cancer patients from Kenya. Breast Cancer Res. 2021;23(1):68. doi: 10.1186/s13058-021-01446-3
https://doi.org/10.1186/s13058-021-01446...
,3030. Cotterchio M, Kreiger N, Theis B, Sloan M, Bahl S. Hormonal factors and the risk of breast cancer according to estrogen- and progesterone-receptor subgroup. Cancer Epidemiol Biomarkers Prev. 2003;12(10):1053-60.

31. Althuis MD, Fergenbaum JH, Garcia-Closas M, Brinton LA, Madigan MP, Sherman ME. Etiology of hormone receptor-defined breast cancer: a systematic review of the literature. Cancer Epidemiol Biomarkers Prev. 2004;13(10):1558-68.
-3232. Yang XR, Sherman ME, Rimm DL, Lissowska J, Brinton LA, Peplonska B, et al. Differences in risk factors for breast cancer molecular subtypes in a population-based study. Cancer Epidemiol Biomarkers Prev. 2007;16(3):439-43. doi: 10.1158/1055-9965.EPI-06-0806
https://doi.org/10.1158/1055-9965.EPI-06...
,3434. Tamimi RM, Colditz GA, Hazra A, Baer HJ, Hankinson SE, Rosner B, et al. Traditional breast cancer risk factors in relation to molecular subtypes of breast cancer. Breast Cancer Res Treat. 2011;131(1):159-67. doi: 10.1007/s10549-011-1702-0
https://doi.org/10.1007/s10549-011-1702-...
One study has found that a later age at menopause represents a higher risk for developing BC, but does not relate this event with any specific subtype of BC. However, other studies have found a relationship between late age at menopause with greater risk of ER+, ER-, PR+, PR -, Luminal B, Luminal A, HER2+, HER2- and triple negative; moreover, late age at menarche was related with a reduced risk of HER2. An earlier age at menopause was related to a higher risk of triple negative BC by one study, a reduced risk only for ductal carcinoma in situ by another and a minor risk for all histological subtypes of BC, except for ductal carcinoma in situ.22. Korzets Y, Yariv O, Mutai R, Moore A, Shochat T, Yerushalmi R, et al. The impact of endogenous estrogen exposures on the characteristics and outcomes of estrogen receptor positive, early breast cancer. Discov Oncol. 2021;12(1):26. doi: 10.1007/s12672-021-00420-x
https://doi.org/10.1007/s12672-021-00420...
,55. Li H, Sun X, Miller E, Wang Q, Tao P, Liu L, et al. BMI, reproductive factors, and breast cancer molecular subtypes: a case-control study and meta-analysis. J Epidemiol. 2017;27(4):143-51. doi: 10.1016/j.je.2016.05.002
https://doi.org/10.1016/j.je.2016.05.002...
,88. Chen L, Li CI, Tang MT, Porter P, Hill DA, Wiggins CL, et al. Reproductive factors and risk of luminal, HER2-overexpressing, and triple-negative breast cancer among multiethnic women. Cancer Epidemiol Biomarkers Prev. 2016;25(9):1297-304. doi: 10.1158/1055-9965.EPI-15-1104
https://doi.org/10.1158/1055-9965.EPI-15...
,1515. Martinez ME, Wertheim BC, Natarajan L, Schwab R, Bondy M, Daneri-Navarro A, et al. Reproductive factors, heterogeneity, and breast tumor subtypes in women of Mexican descent. Cancer Epidemiol Biomarkers Prev. 2013;22(10):1853-61. doi: 10.1158/1055-9965.EPI-13-0560
https://doi.org/10.1158/1055-9965.EPI-13...
,1818. Cui Y, Deming-Halverson SL, Shrubsole MJ, Beeghly-Fadiel A, Fair AM, Sanderson M, et al. Associations of hormone-related factors with breast cancer risk according to hormone receptor status among white and African American women. Clin Breast Cancer. 2014;14(6):417-25. doi: 10.1016/j.clbc.2014.04.003
https://doi.org/10.1016/j.clbc.2014.04.0...

19. Rosato V, Bosetti C, Negri E, Talamini R, Dal Maso L, Malvezzi M, et al. Reproductive and hormonal factors, family history, and breast cancer according to the hormonal receptor status. Eur J Cancer Prev. 2014;23(5):412-7. doi: 10.1097/CEJ.0b013e3283639f7a
https://doi.org/10.1097/CEJ.0b013e328363...

20. O'Brien KM, Sun J, Sandler DP, DeRoo LA, Weinberg CR. Risk factors for young-onset invasive and in situ breast cancer. Cancer Causes Control. 2015;26(12):1771-8. doi: 10.1007/s10552-015-0670-9
https://doi.org/10.1007/s10552-015-0670-...

21. Sisti JS, Collins LC, Beck AH, Tamimi RM, Rosner BA, Eliassen AH. Reproductive risk factors in relation to molecular subtypes of breast cancer: results from the nurses' health studies. Int J Cancer. 2016;138(10):2346-56. doi: 10.1002/ijc.29968
https://doi.org/10.1002/ijc.29968...

22. Ellingjord-Dale M, Vos L, Tretli S, Hofvind S, Dos-Santos-Silva I, Ursin G. Parity, hormones and breast cancer subtypes - results from a large nested case-control study in a national screening program. Breast Cancer Res. 2017;19(1):10. doi: 10.1186/s13058-016-0798-x
https://doi.org/10.1186/s13058-016-0798-...

23. Mullooly M, Khodr ZG, Dallal CM, Nyante SJ, Sherman ME, Falk R, et al. Epidemiologic risk factors for in situ and invasive breast cancers among postmenopausal women in the National Institutes of Health-AARP Diet and Health Study. Am J Epidemiol. 2017;186(12):1329-40. doi: 10.1093/aje/kwx206
https://doi.org/10.1093/aje/kwx206...

24. Soewoto W, Mudigdo A, Aryandono T, Dirgahayu P. Correlation between duration of estrogen exposure with grading of breast cancer. Bali Med J. 2018;7(3):778-81.

25. John EM, Phipps AI, Hines LM, Koo J, Ingles SA, Baumgartner KB, et al. Menstrual and reproductive characteristics and breast cancer risk by hormone receptor status and ethnicity: The Breast Cancer Etiology in Minorities study. Int J Cancer. 2020;147(7):1808-22. doi: 10.1002/ijc.32923
https://doi.org/10.1002/ijc.32923...
-2626. Rojas-Lima E, Gamboa-Loira B, Cebrián ME, Rothenberg SJ, López-Carrillo L. A cumulative index of exposure to endogenous estrogens and breast cancer by molecular subtypes in northern Mexican women. Breast Cancer Res Treat. 2020;180(3):791-800. doi: 10.1007/s10549-020-05562-0
https://doi.org/10.1007/s10549-020-05562...
,2828. Sayed S, Fan S, Moloo Z, Wasike R, Bird P, Saleh M, et al. Breast cancer risk factors in relation to molecular subtypes in breast cancer patients from Kenya. Breast Cancer Res. 2021;23(1):68. doi: 10.1186/s13058-021-01446-3
https://doi.org/10.1186/s13058-021-01446...
,3333. Phipps AI, Chlebowski RT, Prentice R, McTiernan A, Wactawski-Wende J, Kuller LH, et al. Reproductive history and oral contraceptive use in relation to risk of triple-negative breast cancer. J Natl Cancer Inst. 2011;103(6):470-7. doi: 10.1093/jnci/djr030
https://doi.org/10.1093/jnci/djr030...
,3434. Tamimi RM, Colditz GA, Hazra A, Baer HJ, Hankinson SE, Rosner B, et al. Traditional breast cancer risk factors in relation to molecular subtypes of breast cancer. Breast Cancer Res Treat. 2011;131(1):159-67. doi: 10.1007/s10549-011-1702-0
https://doi.org/10.1007/s10549-011-1702-...

Discussion

Most of the analyzed studies have found a relationship between early age at menarche and late age at menopause with certain subtypes of BC, mainly, PR+, ER+, luminal, and HER-2 subtypes of tumors. However, some studies have found a contradictory relationship between these events and BC subtypes, and one study did not find any relationship.

Finding a relationship between early age at menarche and late age at menopause with some BC subtypes was an expected result since a longer exposure to estrogen could imply a greater risk of BC, as previously described in many studies, including a systematic review and meta-analysis conducted in 2012. For sure, this search found that all BC subtypes, with slight variations among them, occurred more frequently in patients who had an earlier age at menarche and more advanced age at menopause.66. Collaborative Group on Hormonal Factors in Breast Cancer. Menarche, menopause, and breast cancer risk: individual participant meta-analysis, including 118 964 women with breast cancer from 117 epidemiological studies. Lancet Oncol. 2012;13(11):1141-51. doi: 10.1016/S1470-2045(12)70425-4
https://doi.org/10.1016/S1470-2045(12)70...

Nonetheless, didn’t find a relationship or found contradictory relationships between the earlier age at menarche, late age at menopause and some BC subtypes, which was unexpected. This could be due to the presence of confounding factors that would influence more or less importantly the risk of developing BC.

Indeed, there are some non-modifiable risk factors such as the presence of BRCA1 and BRCA2 genes and also modifiable risk factors, such as environmental exposure to carcinogens, psychological stress and tobacco that can show adverse effects through hormonal and non-hormonal pathways, determining variations in the ages of the first and last menstruation and then, through direct and indirect effects, influence the development of BC.3535. Chang-Claude J, Andrieu N, Rookus M, Brohet R, Antoniou AC, Peock S, et al. Age at menarche and menopause and breast cancer risk in the International BRCA1/2 Carrier Cohort Study. Cancer Epidemiol Biomarkers Prev. 2007;16(4):740-6. doi: 10.1158/1055-9965.EPI-06-0829
https://doi.org/10.1158/1055-9965.EPI-06...

36. Forman MR, Mangini LD, Thelus-Jean R, Hayward MD. Life-course origins of the ages at menarche and menopause. Adolesc Health Med Ther. 2013;4:1-21. doi: 10.2147/AHMT.S15946
https://doi.org/10.2147/AHMT.S15946...
-3737. Guo L, Peng C, Xu H, Wilson A, Li PH, Wang H, et al. Age at menarche and prevention of hypertension through lifestyle in young Chinese adult women: result from project ELEFANT. BMC Womens Health. 2018;18(1):182. doi: 10.1186/s12905-018-0677-y
https://doi.org/10.1186/s12905-018-0677-...

It is also important to consider the role of locoregional factors on the ages at menarche and menopause and the risk of developing BC. For sure, different prevalences of BC were observed between different developed and developing countries, which may be related to nutritional factors, access to medical care, prevention policies, better therapies and even parity.3838. Tiezzi DG. [Breast cancer: a future challenge for the health system in developing countries]. Rev Bras Ginecol Obstet. 2010;32(6):257-9. Portuguese.,3939. Sousa AC. Idade da menopausa e da menarca: inquérito populacional em mulheres climatéricas [dissertação]. São Luís: Universidade Federal do Maranhão; 2012 [cited 2023 Nov 26]. Available from: https://tedebc.ufma.br/jspui/bitstream/tede/1175/1/DISSERTACAO%20ANA%20CLEIDE.pdf
https://tedebc.ufma.br/jspui/bitstream/t...

Another fact to be highlighted is the diversity found regarding the definition of early age at menarche and late age at menopause. Indeed, there isn’t a specific age of early menarche and of late menopause defined in the literature, since they vary with temporal and social factors.4040. Ulubay M, Fidan U, Ozturk M. The decreasing age of menarche in Turkey: global warming, socioeconomic development, and environmental factors. Eur Rev Med Pharmacol Sci. 2023;27(14):6780-4. doi: 10.26355/eurrev_202307_33148
https://doi.org/10.26355/eurrev_202307_3...
,4141. Ferreira IC, Silva SS, Almeida RS. Menopausa, sinais e sintomas e seus aspectos psicológicos em mulheres sem uso de reposição hormonal. Ensaios Ciênc Ciênc Biol Agrár Saúde. 2015;19(2):60-4. doi: 10.17921/1415-6938.2015v19n2p%25p
https://doi.org/10.17921/1415-6938.2015v...
In this way, our study found ages of early menarche and late menopause that varied from 9 to 13 years and 45 to 60 years, respectively, which could have been confounding factors in establishing the relationship between these events and the risk of developing BC.

Ethnicity has also been shown to be related to the risk of developing certain subtypes of BC.2525. John EM, Phipps AI, Hines LM, Koo J, Ingles SA, Baumgartner KB, et al. Menstrual and reproductive characteristics and breast cancer risk by hormone receptor status and ethnicity: The Breast Cancer Etiology in Minorities study. Int J Cancer. 2020;147(7):1808-22. doi: 10.1002/ijc.32923
https://doi.org/10.1002/ijc.32923...
African-American women who had earlier ages at menarche and late ages at menopause, have been found to have a higher risk of developing ER-, PR- and triple negative tumors.1818. Cui Y, Deming-Halverson SL, Shrubsole MJ, Beeghly-Fadiel A, Fair AM, Sanderson M, et al. Associations of hormone-related factors with breast cancer risk according to hormone receptor status among white and African American women. Clin Breast Cancer. 2014;14(6):417-25. doi: 10.1016/j.clbc.2014.04.003
https://doi.org/10.1016/j.clbc.2014.04.0...
Non-Hispanic Whites and Hispanic American women, who had a late age at menarche and an earlier age at menopause showed a reduced risk of HR+ and HR - BC subtypes.2525. John EM, Phipps AI, Hines LM, Koo J, Ingles SA, Baumgartner KB, et al. Menstrual and reproductive characteristics and breast cancer risk by hormone receptor status and ethnicity: The Breast Cancer Etiology in Minorities study. Int J Cancer. 2020;147(7):1808-22. doi: 10.1002/ijc.32923
https://doi.org/10.1002/ijc.32923...

A great heterogeneity in the classification of BC subtypes between the analyzed studies was also found. Some studies mentioned only 2 and others up to twelve subtypes. Furthermore, most studies mentioned only molecular subtypes of BC, minimizing the discussion on histological subtypes. Thus, despite the existence of a very detailed classification, as the one proposed by the WHO; in general, the studies adapted the classification of subtypes to their scope of analysis and discussion, making comparisons and correlations between the studies difficult.

An important limitation of our study was that data identification underwent reformulations throughout the review process, which may have introduced some bias. However, we believe that the articles designated as “exclusive reanalysis” would be wasted although they are relevant to the objective of this review, which was the reason why they were included. Regarding data extraction, most studies were nonspecific, consequently, some results remained not fully analyzed by the original authors, thus limiting the establishment of relevant relationships.

Conclusion

A relationship between early age at menarche and advanced age at menopause was observed with some subtypes of BC, since factors such as genes, ethnicity, environmental and locoregional conditions influence this relationship and must be considered in its interpretation.

y, years; BMI, Body Mass Index; HR, Hormone receptor, ER, Estrogen Receptor, PR, Progesterone receptor, HER2, Protein receptor; DCIS, Ductal Carcinoma in situ; LCIS, Lobular Carcinoma in situ, Luminal A, ER and PR present, without HER, low expression of Ki-67; Luminal B, ER and PR present, without HER, high expression of Ki-67; HER-2, ER and PR absent; TN, Triple Negative, ER, PR and HER absent; Stage III, higher grade of tumor that still resectable.

References

  • 1
    da Silva BB, Sousa-Esteves FC, Martins RS, Salha CP, Paiva-Melo BN, Moura CS, et al. Clinical and epidemiological profile of women with breast cancer managed in a public referral hospital in northeastern Brazil. Eur J Gynaecol Oncol. 2016;37(6):814-6.
  • 2
    Korzets Y, Yariv O, Mutai R, Moore A, Shochat T, Yerushalmi R, et al. The impact of endogenous estrogen exposures on the characteristics and outcomes of estrogen receptor positive, early breast cancer. Discov Oncol. 2021;12(1):26. doi: 10.1007/s12672-021-00420-x
    » https://doi.org/10.1007/s12672-021-00420-x
  • 3
    Silva PA, Riul SS. Câncer de mama: fatores de risco e detecção precoce. Rev Bras Enferm. 2011;64(6):1016-21. doi: 10.1590/S0034-71672011000600005
    » https://doi.org/10.1590/S0034-71672011000600005
  • 4
    Su CH, Chang WS, Hu PS, Hsiao CL, Ji HX, Liao CH, et al. Contribution of DNA double-strand break repair gene XRCC3 genotypes to triple-negative breast cancer risk. Cancer Genom Proteom. 2015;12(6):359-67.
  • 5
    Li H, Sun X, Miller E, Wang Q, Tao P, Liu L, et al. BMI, reproductive factors, and breast cancer molecular subtypes: a case-control study and meta-analysis. J Epidemiol. 2017;27(4):143-51. doi: 10.1016/j.je.2016.05.002
    » https://doi.org/10.1016/j.je.2016.05.002
  • 6
    Collaborative Group on Hormonal Factors in Breast Cancer. Menarche, menopause, and breast cancer risk: individual participant meta-analysis, including 118 964 women with breast cancer from 117 epidemiological studies. Lancet Oncol. 2012;13(11):1141-51. doi: 10.1016/S1470-2045(12)70425-4
    » https://doi.org/10.1016/S1470-2045(12)70425-4
  • 7
    Actis AM, Bergoc RM, Quartucci Á, Outomuro D. Factores de riesgo convencionales y emergentes en cáncer de mama: un estudio en pacientes posmenopáusicas. Rev Chil Obstet Ginecol. 2009;74(3):135-42. doi: 10.4067/S0717-75262009000300002
    » https://doi.org/10.4067/S0717-75262009000300002
  • 8
    Chen L, Li CI, Tang MT, Porter P, Hill DA, Wiggins CL, et al. Reproductive factors and risk of luminal, HER2-overexpressing, and triple-negative breast cancer among multiethnic women. Cancer Epidemiol Biomarkers Prev. 2016;25(9):1297-304. doi: 10.1158/1055-9965.EPI-15-1104
    » https://doi.org/10.1158/1055-9965.EPI-15-1104
  • 9
    Coignet MV, Zirpoli GR, Roberts MR, Khoury T, Bandera EV, Zhu Q, et al. Genetic variations, reproductive aging, and breast cancer risk in African American and European American women: The Women's Circle of Health Study. PLoS One. 2017;12(10):e0187205. doi: 10.1371/journal.pone.0187205
    » https://doi.org/10.1371/journal.pone.0187205
  • 10
    Sun YS, Zhao Z, Yang ZN, Xu F, Lu HJ, Zhu ZY, et al. Risk factors and preventions of breast cancer. Int J Biol Sci. 2017;13(11):1387-97. doi: 10.7150/ijbs.21635
    » https://doi.org/10.7150/ijbs.21635
  • 11
    Wysocka J. New WHO classification of breast tumours - as published in 2019. Nowotwory J Oncol. 2020;70(6):250-2. doi: 10.5603/NJO.a2020.0038
    » https://doi.org/10.5603/NJO.a2020.0038
  • 12
    Peters MD, Marnie C, Tricco AC, Pollock D, Munn Z, Alexander L, et al. Updated methodological guidance for the conduct of scoping reviews. JBI Evid Implement. 2021;19(1):3-10.
  • 13
    Anderson JK, Howarth E, Vainre M, Humphrey A, Jones PB, Ford TJ. Advancing methodology for scoping reviews: recommendations arising from a scoping literature review (SLR) to inform transformation of Children and Adolescent Mental Health Services. BMC Med Res Methodol. 2020;20(1):242. doi: 10.1186/s12874-020-01127-3
    » https://doi.org/10.1186/s12874-020-01127-3
  • 14
    Tricco AC, Lillie E, Zarin W, O'Brien KK, Colquhoun H, Levac D, et al. PRISMA Extension for Scoping Reviews (PRISMA-ScR): checklist and explanation. Ann Intern Med. 2018;169(7):467-73. doi: 10.7326/M18-0850
    » https://doi.org/10.7326/M18-0850
  • 15
    Martinez ME, Wertheim BC, Natarajan L, Schwab R, Bondy M, Daneri-Navarro A, et al. Reproductive factors, heterogeneity, and breast tumor subtypes in women of Mexican descent. Cancer Epidemiol Biomarkers Prev. 2013;22(10):1853-61. doi: 10.1158/1055-9965.EPI-13-0560
    » https://doi.org/10.1158/1055-9965.EPI-13-0560
  • 16
    Ritte R, Tikk K, Lukanova A, Tjønneland A, Olsen A, Overvad K, et al. Reproductive factors and risk of hormone receptor positive and negative breast cancer: a cohort study. BMC Cancer. 2013;13:584. doi: 10.1186/1471-2407-13-584
    » https://doi.org/10.1186/1471-2407-13-584
  • 17
    Turkoz FP, Solak M, Petekkaya I, Keskin O, Kertmen N, Sarici F, et al. Association between common risk factors and molecular subtypes in breast cancer patients. Breast. 2013;22(3):344-50. doi: 10.1016/j.breast.2012.08.005
    » https://doi.org/10.1016/j.breast.2012.08.005
  • 18
    Cui Y, Deming-Halverson SL, Shrubsole MJ, Beeghly-Fadiel A, Fair AM, Sanderson M, et al. Associations of hormone-related factors with breast cancer risk according to hormone receptor status among white and African American women. Clin Breast Cancer. 2014;14(6):417-25. doi: 10.1016/j.clbc.2014.04.003
    » https://doi.org/10.1016/j.clbc.2014.04.003
  • 19
    Rosato V, Bosetti C, Negri E, Talamini R, Dal Maso L, Malvezzi M, et al. Reproductive and hormonal factors, family history, and breast cancer according to the hormonal receptor status. Eur J Cancer Prev. 2014;23(5):412-7. doi: 10.1097/CEJ.0b013e3283639f7a
    » https://doi.org/10.1097/CEJ.0b013e3283639f7a
  • 20
    O'Brien KM, Sun J, Sandler DP, DeRoo LA, Weinberg CR. Risk factors for young-onset invasive and in situ breast cancer. Cancer Causes Control. 2015;26(12):1771-8. doi: 10.1007/s10552-015-0670-9
    » https://doi.org/10.1007/s10552-015-0670-9
  • 21
    Sisti JS, Collins LC, Beck AH, Tamimi RM, Rosner BA, Eliassen AH. Reproductive risk factors in relation to molecular subtypes of breast cancer: results from the nurses' health studies. Int J Cancer. 2016;138(10):2346-56. doi: 10.1002/ijc.29968
    » https://doi.org/10.1002/ijc.29968
  • 22
    Ellingjord-Dale M, Vos L, Tretli S, Hofvind S, Dos-Santos-Silva I, Ursin G. Parity, hormones and breast cancer subtypes - results from a large nested case-control study in a national screening program. Breast Cancer Res. 2017;19(1):10. doi: 10.1186/s13058-016-0798-x
    » https://doi.org/10.1186/s13058-016-0798-x
  • 23
    Mullooly M, Khodr ZG, Dallal CM, Nyante SJ, Sherman ME, Falk R, et al. Epidemiologic risk factors for in situ and invasive breast cancers among postmenopausal women in the National Institutes of Health-AARP Diet and Health Study. Am J Epidemiol. 2017;186(12):1329-40. doi: 10.1093/aje/kwx206
    » https://doi.org/10.1093/aje/kwx206
  • 24
    Soewoto W, Mudigdo A, Aryandono T, Dirgahayu P. Correlation between duration of estrogen exposure with grading of breast cancer. Bali Med J. 2018;7(3):778-81.
  • 25
    John EM, Phipps AI, Hines LM, Koo J, Ingles SA, Baumgartner KB, et al. Menstrual and reproductive characteristics and breast cancer risk by hormone receptor status and ethnicity: The Breast Cancer Etiology in Minorities study. Int J Cancer. 2020;147(7):1808-22. doi: 10.1002/ijc.32923
    » https://doi.org/10.1002/ijc.32923
  • 26
    Rojas-Lima E, Gamboa-Loira B, Cebrián ME, Rothenberg SJ, López-Carrillo L. A cumulative index of exposure to endogenous estrogens and breast cancer by molecular subtypes in northern Mexican women. Breast Cancer Res Treat. 2020;180(3):791-800. doi: 10.1007/s10549-020-05562-0
    » https://doi.org/10.1007/s10549-020-05562-0
  • 27
    Ulgen A, Gurkut O, Li W. Potential predictive factors for breast cancer subtypes from a North Cyprus Cohort Analysis. Cyprus J Med Sci. 2021;5(4):339-49. doi: 10.5152/cjms.2020.2291
    » https://doi.org/10.5152/cjms.2020.2291
  • 28
    Sayed S, Fan S, Moloo Z, Wasike R, Bird P, Saleh M, et al. Breast cancer risk factors in relation to molecular subtypes in breast cancer patients from Kenya. Breast Cancer Res. 2021;23(1):68. doi: 10.1186/s13058-021-01446-3
    » https://doi.org/10.1186/s13058-021-01446-3
  • 29
    Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, et al. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA. 2006;295(21):2492-502. doi: 10.1001/jama.295.21.2492
    » https://doi.org/10.1001/jama.295.21.2492
  • 30
    Cotterchio M, Kreiger N, Theis B, Sloan M, Bahl S. Hormonal factors and the risk of breast cancer according to estrogen- and progesterone-receptor subgroup. Cancer Epidemiol Biomarkers Prev. 2003;12(10):1053-60.
  • 31
    Althuis MD, Fergenbaum JH, Garcia-Closas M, Brinton LA, Madigan MP, Sherman ME. Etiology of hormone receptor-defined breast cancer: a systematic review of the literature. Cancer Epidemiol Biomarkers Prev. 2004;13(10):1558-68.
  • 32
    Yang XR, Sherman ME, Rimm DL, Lissowska J, Brinton LA, Peplonska B, et al. Differences in risk factors for breast cancer molecular subtypes in a population-based study. Cancer Epidemiol Biomarkers Prev. 2007;16(3):439-43. doi: 10.1158/1055-9965.EPI-06-0806
    » https://doi.org/10.1158/1055-9965.EPI-06-0806
  • 33
    Phipps AI, Chlebowski RT, Prentice R, McTiernan A, Wactawski-Wende J, Kuller LH, et al. Reproductive history and oral contraceptive use in relation to risk of triple-negative breast cancer. J Natl Cancer Inst. 2011;103(6):470-7. doi: 10.1093/jnci/djr030
    » https://doi.org/10.1093/jnci/djr030
  • 34
    Tamimi RM, Colditz GA, Hazra A, Baer HJ, Hankinson SE, Rosner B, et al. Traditional breast cancer risk factors in relation to molecular subtypes of breast cancer. Breast Cancer Res Treat. 2011;131(1):159-67. doi: 10.1007/s10549-011-1702-0
    » https://doi.org/10.1007/s10549-011-1702-0
  • 35
    Chang-Claude J, Andrieu N, Rookus M, Brohet R, Antoniou AC, Peock S, et al. Age at menarche and menopause and breast cancer risk in the International BRCA1/2 Carrier Cohort Study. Cancer Epidemiol Biomarkers Prev. 2007;16(4):740-6. doi: 10.1158/1055-9965.EPI-06-0829
    » https://doi.org/10.1158/1055-9965.EPI-06-0829
  • 36
    Forman MR, Mangini LD, Thelus-Jean R, Hayward MD. Life-course origins of the ages at menarche and menopause. Adolesc Health Med Ther. 2013;4:1-21. doi: 10.2147/AHMT.S15946
    » https://doi.org/10.2147/AHMT.S15946
  • 37
    Guo L, Peng C, Xu H, Wilson A, Li PH, Wang H, et al. Age at menarche and prevention of hypertension through lifestyle in young Chinese adult women: result from project ELEFANT. BMC Womens Health. 2018;18(1):182. doi: 10.1186/s12905-018-0677-y
    » https://doi.org/10.1186/s12905-018-0677-y
  • 38
    Tiezzi DG. [Breast cancer: a future challenge for the health system in developing countries]. Rev Bras Ginecol Obstet. 2010;32(6):257-9. Portuguese.
  • 39
    Sousa AC. Idade da menopausa e da menarca: inquérito populacional em mulheres climatéricas [dissertação]. São Luís: Universidade Federal do Maranhão; 2012 [cited 2023 Nov 26]. Available from: https://tedebc.ufma.br/jspui/bitstream/tede/1175/1/DISSERTACAO%20ANA%20CLEIDE.pdf
    » https://tedebc.ufma.br/jspui/bitstream/tede/1175/1/DISSERTACAO%20ANA%20CLEIDE.pdf
  • 40
    Ulubay M, Fidan U, Ozturk M. The decreasing age of menarche in Turkey: global warming, socioeconomic development, and environmental factors. Eur Rev Med Pharmacol Sci. 2023;27(14):6780-4. doi: 10.26355/eurrev_202307_33148
    » https://doi.org/10.26355/eurrev_202307_33148
  • 41
    Ferreira IC, Silva SS, Almeida RS. Menopausa, sinais e sintomas e seus aspectos psicológicos em mulheres sem uso de reposição hormonal. Ensaios Ciênc Ciênc Biol Agrár Saúde. 2015;19(2):60-4. doi: 10.17921/1415-6938.2015v19n2p%25p
    » https://doi.org/10.17921/1415-6938.2015v19n2p%25p

Edited by

Associate Editor

Andréa Pires Souto Damin (https://orcid.org/0000-0002-5246-7388) Universidade Federal de Ciências da Saúde de Porto Alegre, Porto Alegre, RS, Brazil

Publication Dates

  • Publication in this collection
    30 Sept 2024
  • Date of issue
    2024

History

  • Received
    27 Nov 2023
  • Accepted
    08 Feb 2024
Federação Brasileira das Sociedades de Ginecologia e Obstetrícia Av. Brigadeiro Luís Antônio, 3421, sala 903 - Jardim Paulista, 01401-001 São Paulo SP - Brasil, Tel. (55 11) 5573-4919 - Rio de Janeiro - RJ - Brazil
E-mail: editorial.office@febrasgo.org.br